Semin Neurol 2018; 38(03): 379-391
DOI: 10.1055/s-0038-1660820
Review Article
Thieme Medical Publishers 333 Seventh Avenue, New York, NY 10001, USA.

Infection, Immunodeficiency, and Inflammatory Diseases in Autoimmune Neurology

Amanda L. Piquet
1   Department of Neurology, University of Colorado, Aurora, Colorado
,
Stacey L. Clardy
2   Department of Neurology, University of Utah, Salt Lake City, Utah
› Author Affiliations
Further Information

Publication History

Publication Date:
16 July 2018 (online)

Abstract

When patients present with neurological syndromes, such as encephalopathy/encephalitis, meningitis, and/or myelopathy/myelitis, the differential diagnosis is often broad, including infectious, inflammatory, autoimmune, vascular, and neoplastic etiologies. Just with inflammatory and autoimmune etiologies alone, there are numerous causative diseases. A comprehensive history and physical examination investigating for extraneurologic manifestations of immune-mediated disease is often necessary. Moreover, evaluating for an underlying infection and/or immunodeficiency becomes a critical aspect to the workup. This article will focus on the association of viral infections and dysregulation of the immune system as triggers of autoimmunity, in addition to various systemic inflammatory diseases that can cause neurological disease either with or without an established rheumatological disorder.

 
  • References

  • 1 Shapira Y, Agmon-Levin N, Shoenfeld Y. Defining and analyzing geoepidemiology and human autoimmunity. J Autoimmun 2010; 34 (03) J168-J177
  • 2 Hynson JL, Kornberg AJ, Coleman LT, Shield L, Harvey AS, Kean MJ. Clinical and neuroradiologic features of acute disseminated encephalomyelitis in children. Neurology 2001; 56 (10) 1308-1312
  • 3 Kipps A, Dick G, Moodie JW. Measles and the central nervous system. Lancet 1983; 2 (8364): 1406-1410
  • 4 Karussis D, Petrou P. The spectrum of post-vaccination inflammatory CNS demyelinating syndromes. Autoimmun Rev 2014; 13 (03) 215-224
  • 5 Armangue T, Leypoldt F, Málaga I. , et al. Herpes simplex virus encephalitis is a trigger of brain autoimmunity. Ann Neurol 2014; 75 (02) 317-323
  • 6 Linnoila JJ, Binnicker MJ, Majed M, Klein CJ, McKeon A. CSF herpes virus and autoantibody profiles in the evaluation of encephalitis. Neurol Neuroimmunol Neuroinflamm 2016; 3 (04) e245
  • 7 Schäbitz WR, Rogalewski A, Hagemeister C, Bien CG. VZV brainstem encephalitis triggers NMDA receptor immunoreaction. Neurology 2014; 83 (24) 2309-2311
  • 8 Getts DR, Chastain EM, Terry RL, Miller SD. Virus infection, antiviral immunity, and autoimmunity. Immunol Rev 2013; 255 (01) 197-209
  • 9 Ercolini AM, Miller SD. The role of infections in autoimmune disease. Clin Exp Immunol 2009; 155 (01) 1-15
  • 10 Fujinami RS, Oldstone MB, Wroblewska Z, Frankel ME, Koprowski H. Molecular mimicry in virus infection: cross-reaction of measles virus phosphoprotein or of herpes simplex virus protein with human intermediate filaments. Proc Natl Acad Sci U S A 1983; 80 (08) 2346-2350
  • 11 Cusick MF, Libbey JE, Fujinami RS. Molecular mimicry as a mechanism of autoimmune disease. Clin Rev Allergy Immunol 2012; 42 (01) 102-111
  • 12 Kirvan CA, Swedo SE, Heuser JS, Cunningham MW. Mimicry and autoantibody-mediated neuronal cell signaling in Sydenham chorea. Nat Med 2003; 9 (07) 914-920
  • 13 Ang CW, Jacobs BC, Laman JD. The Guillain-Barré syndrome: a true case of molecular mimicry. Trends Immunol 2004; 25 (02) 61-66
  • 14 Araujo AQ, Silva MT. The HTLV-1 neurological complex. Lancet Neurol 2006; 5 (12) 1068-1076
  • 15 Mameli G, Cocco E, Frau J, Marrosu MG, Sechi LA. Epstein Barr Virus and Mycobacterium avium subsp. paratuberculosis peptides are recognized in sera and cerebrospinal fluid of MS patients. Sci Rep 2016; 6: 22401
  • 16 Husby G, van de Rijn I, Zabriskie JB, Abdin ZH, Williams Jr RC. Antibodies reacting with cytoplasm of subthalamic and caudate nuclei neurons in chorea and acute rheumatic fever. J Exp Med 1976; 144 (04) 1094-1110
  • 17 Hoffman KL, Hornig M, Yaddanapudi K, Jabado O, Lipkin WI. A murine model for neuropsychiatric disorders associated with group A beta-hemolytic streptococcal infection. J Neurosci 2004; 24 (07) 1780-1791
  • 18 Bronze MS, Dale JB. Epitopes of streptococcal M proteins that evoke antibodies that cross-react with human brain. J Immunol 1993; 151 (05) 2820-2828
  • 19 Jolles S. The variable in common variable immunodeficiency: a disease of complex phenotypes. J Allergy Clin Immunol Pract 2013; 1 (06) 545-556 , quiz 557
  • 20 Conley ME, Notarangelo LD, Etzioni A. ; Representing PAGID (Pan-American Group for Immunodeficiency) and ESID (European Society for Immunodeficiencies). Diagnostic criteria for primary immunodeficiencies. Clin Immunol 1999; 93 (03) 190-197
  • 21 Schubert RD, Wilson MR. A tale of two approaches: how metagenomics and proteomics are shaping the future of encephalitis diagnostics. Curr Opin Neurol 2015; 28 (03) 283-287
  • 22 Wilson MR, Naccache SN, Samayoa E. , et al. Actionable diagnosis of neuroleptospirosis by next-generation sequencing. N Engl J Med 2014; 370 (25) 2408-2417
  • 23 Quan PL, Wagner TA, Briese T. , et al. Astrovirus encephalitis in boy with X-linked agammaglobulinemia. Emerg Infect Dis 2010; 16 (06) 918-925
  • 24 Naccache SN, Peggs KS, Mattes FM. , et al. Diagnosis of neuroinvasive astrovirus infection in an immunocompromised adult with encephalitis by unbiased next-generation sequencing. Clin Infect Dis 2015; 60 (06) 919-923
  • 25 Bonilla FA, Barlan I, Chapel H. , et al. International Consensus Document (ICON): common variable immunodeficiency disorders. J Allergy Clin Immunol Pract 2016; 4 (01) 38-59
  • 26 Boursiquot JN, Gérard L, Malphettes M. , et al; DEFI Study Group. Granulomatous disease in CVID: retrospective analysis of clinical characteristics and treatment efficacy in a cohort of 59 patients. J Clin Immunol 2013; 33 (01) 84-95
  • 27 Morimoto Y, Routes JM. Granulomatous disease in common variable immunodeficiency. Curr Allergy Asthma Rep 2005; 5 (05) 370-375
  • 28 Ardeniz O, Cunningham-Rundles C. Granulomatous disease in common variable immunodeficiency. Clin Immunol 2009; 133 (02) 198-207
  • 29 Arnold DF, Wiggins J, Cunningham-Rundles C, Misbah SA, Chapel HM. Granulomatous disease: distinguishing primary antibody disease from sarcoidosis. Clin Immunol 2008; 128 (01) 18-22
  • 30 Misbah SA, Spickett GP, Esiri MM. , et al. Recurrent intra-cranial granulomata presenting as space-occupying lesions in a patient with common variable immunodeficiency. Postgrad Med J 1992; 68 (799) 359-362
  • 31 Nguyen JT, Green A, Wilson MR, DeRisi JL, Gundling K. Neurologic complications of common variable immunodeficiency. J Clin Immunol 2016; 36 (08) 793-800
  • 32 Shiboski CH, Shiboski SC, Seror R. , et al; International Sjögren's Syndrome Criteria Working Group. 2016 American College of Rheumatology/European League Against Rheumatism Classification Criteria for Primary Sjögren's Syndrome: A consensus and data-driven methodology involving three international patient cohorts. Arthritis Rheumatol 2017; 69 (01) 35-45
  • 33 Vitali C, Bombardieri S, Jonsson R. , et al; European Study Group on Classification Criteria for Sjögren's Syndrome. Classification criteria for Sjögren's syndrome: a revised version of the European criteria proposed by the American-European Consensus Group. Ann Rheum Dis 2002; 61 (06) 554-558
  • 34 Delalande S, de Seze J, Fauchais AL. , et al. Neurologic manifestations in primary Sjögren syndrome: a study of 82 patients. Medicine (Baltimore) 2004; 83 (05) 280-291
  • 35 Ramos-Casals M, Solans R, Rosas J. , et al; GEMESS Study Group. Primary Sjögren syndrome in Spain: clinical and immunologic expression in 1010 patients. Medicine (Baltimore) 2008; 87 (04) 210-219
  • 36 Kassan SS, Moutsopoulos HM. Clinical manifestations and early diagnosis of Sjögren syndrome. Arch Intern Med 2004; 164 (12) 1275-1284
  • 37 Morreale M, Marchione P, Giacomini P. , et al. Neurological involvement in primary Sjögren syndrome: a focus on central nervous system. PLoS One 2014; 9 (01) e84605
  • 38 Valtýsdóttir ST, Gudbjörnsson B, Lindqvist U, Hällgren R, Hetta J. Anxiety and depression in patients with primary Sjögren's syndrome. J Rheumatol 2000; 27 (01) 165-169
  • 39 Valtýsdóttir ST, Gudbjörnsson B, Hällgren R, Hetta J. Psychological well-being in patients with primary Sjögren's syndrome. Clin Exp Rheumatol 2000; 18 (05) 597-600
  • 40 Tzarouchi LC, Zikou AK, Tsifetaki N. , et al. White matter water diffusion changes in primary Sjögren syndrome. AJNR Am J Neuroradiol 2014; 35 (04) 680-685
  • 41 Kim SM, Waters P, Vincent A. , et al. Sjogren's syndrome myelopathy: spinal cord involvement in Sjogren's syndrome might be a manifestation of neuromyelitis optica. Mult Scler 2009; 15 (09) 1062-1068
  • 42 Jarius S, Jacobi C, de Seze J. , et al. Frequency and syndrome specificity of antibodies to aquaporin-4 in neurological patients with rheumatic disorders. Mult Scler 2011; 17 (09) 1067-1073
  • 43 Jarius S, Wildemann B. AQP4 antibodies in neuromyelitis optica: diagnostic and pathogenetic relevance. Nat Rev Neurol 2010; 6 (07) 383-392
  • 44 Tobón GJ, Pers JO, Devauchelle-Pensec V, Youinou P. Neurological disorders in primary Sjögren's syndrome. Autoimmune Dis 2012; 2012: 645967
  • 45 Park K, Haberberger RV, Gordon TP, Jackson MW. Antibodies interfering with the type 3 muscarinic receptor pathway inhibit gastrointestinal motility and cholinergic neurotransmission in Sjögren's syndrome. Arthritis Rheum 2011; 63 (05) 1426-1434
  • 46 Rist S, Sellam J, Hachulla E. , et al; Club Rhumatismes et Inflammation. Experience of intravenous immunoglobulin therapy in neuropathy associated with primary Sjögren's syndrome: a national multicentric retrospective study. Arthritis Care Res (Hoboken) 2011; 63 (09) 1339-1344
  • 47 Chen WH, Yeh JH, Chiu HC. Plasmapheresis in the treatment of ataxic sensory neuropathy associated with Sjögren's syndrome. Eur Neurol 2001; 45 (04) 270-274
  • 48 Gottenberg JE, Cinquetti G, Larroche C. , et al; Club Rhumatismes et Inflammations and the French Society of Rheumatology. Efficacy of rituximab in systemic manifestations of primary Sjogren's syndrome: results in 78 patients of the AutoImmune and Rituximab registry. Ann Rheum Dis 2013; 72 (06) 1026-1031
  • 49 Caroyer JM, Manto MU, Steinfeld SD. Severe sensory neuronopathy responsive to infliximab in primary Sjögren's syndrome. Neurology 2002; 59 (07) 1113-1114
  • 50 Gottenberg JE, Ravaud P, Puéchal X. , et al. Effects of hydroxychloroquine on symptomatic improvement in primary Sjögren syndrome: the JOQUER randomized clinical trial. JAMA 2014; 312 (03) 249-258
  • 51 Mariette X, Ravaud P, Steinfeld S. , et al. Inefficacy of infliximab in primary Sjögren's syndrome: results of the randomized, controlled Trial of Remicade in Primary Sjögren's Syndrome (TRIPSS). Arthritis Rheum 2004; 50 (04) 1270-1276
  • 52 D'Cruz DP, Khamashta MA, Hughes GR. Systemic lupus erythematosus. Lancet 2007; 369 (9561): 587-596
  • 53 Bhattacharyya S, Helfgott SM. Neurologic complications of systemic lupus erythematosus, Sjögren syndrome, and rheumatoid arthritis. Semin Neurol 2014; 34 (04) 425-436
  • 54 Cozzani E, Drosera M, Gasparini G, Parodi A. Serology of lupus erythematosus: correlation between immunopathological features and clinical aspects. Autoimmune Dis 2014; 2014: 321359
  • 55 Hochberg MC. Updating the American College of Rheumatology revised criteria for the classification of systemic lupus erythematosus. Arthritis Rheum 1997; 40 (09) 1725
  • 56 Devinsky O, Schein A, Najjar S. Epilepsy associated with systemic autoimmune disorders. Epilepsy Curr 2013; 13 (02) 62-68
  • 57 Appenzeller S, Cendes F, Costallat LT. Epileptic seizures in systemic lupus erythematosus. Neurology 2004; 63 (10) 1808-1812
  • 58 Timlin H, Petri M. Transient ischemic attack and stroke in systemic lupus erythematosus. Lupus 2013; 22 (12) 1251-1258
  • 59 Giannakopoulos B, Krilis SA. The pathogenesis of the antiphospholipid syndrome. N Engl J Med 2013; 368 (11) 1033-1044
  • 60 Hajj-Ali RA, Calabrese LH. Diagnosis and classification of central nervous system vasculitis. J Autoimmun 2014; ;48-49: 149-152
  • 61 John S, Hajj-Ali RA. CNS vasculitis. Semin Neurol 2014; 34 (04) 405-412
  • 62 Chow FC, Marra CM, Cho TA. Cerebrovascular disease in central nervous system infections. Semin Neurol 2011; 31 (03) 286-306
  • 63 Salvarani C, Brown Jr RD, Huston III J, Morris JM, Hunder GG. Treatment of primary CNS vasculitis with rituximab: case report. Neurology 2014; 82 (14) 1287-1288
  • 64 Yates M, Watts RA, Bajema IM. , et al. EULAR/ERA-EDTA recommendations for the management of ANCA-associated vasculitis. Ann Rheum Dis 2016; 75 (09) 1583-1594
  • 65 Evans J, Steel L, Borg F, Dasgupta B. Long-term efficacy and safety of tocilizumab in giant cell arteritis and large vessel vasculitis. RMD Open 2016; 2 (01) e000137
  • 66 Devauchelle-Pensec V, Berthelot JM, Cornec D. , et al. Efficacy of first-line tocilizumab therapy in early polymyalgia rheumatica: a prospective longitudinal study. Ann Rheum Dis 2016; 75 (08) 1506-1510
  • 67 Tavee JO, Stern BJ. Neurosarcoidosis. Clin Chest Med 2015; 36 (04) 643-656
  • 68 Allen RK, Sellars RE, Sandstrom PA. A prospective study of 32 patients with neurosarcoidosis. Sarcoidosis Vasc Diffuse Lung Dis 2003; 20 (02) 118-125
  • 69 Gascón-Bayarri J, Mañá J, Martínez-Yélamos S, Murillo O, Reñé R, Rubio F. Neurosarcoidosis: report of 30 cases and a literature survey. Eur J Intern Med 2011; 22 (06) e125-e132
  • 70 Rybicki BA, Major M, Popovich Jr J, Maliarik MJ, Iannuzzi MC. Racial differences in sarcoidosis incidence: a 5-year study in a health maintenance organization. Am J Epidemiol 1997; 145 (03) 234-241
  • 71 Zajicek JP, Scolding NJ, Foster O. , et al. Central nervous system sarcoidosis--diagnosis and management. QJM 1999; 92 (02) 103-117
  • 72 Agnihotri SP, Singhal T, Stern BJ, Cho TA. Neurosarcoidosis. Semin Neurol 2014; 34 (04) 386-394
  • 73 Stern BJ, Krumholz A, Johns C, Scott P, Nissim J. Sarcoidosis and its neurological manifestations. Arch Neurol 1985; 42 (09) 909-917
  • 74 Chapelon C, Ziza JM, Piette JC. , et al. Neurosarcoidosis: signs, course and treatment in 35 confirmed cases. Medicine (Baltimore) 1990; 69 (05) 261-276
  • 75 Chow E, Troy SB. The differential diagnosis of hypoglycorrhachia in adult patients. Am J Med Sci 2014; 348 (03) 186-190
  • 76 Bridel C, Courvoisier DS, Vuilleumier N, Lalive PH. Cerebrospinal fluid angiotensin-converting enzyme for diagnosis of neurosarcoidosis. J Neuroimmunol 2015; 285: 1-3
  • 77 Nishiyama Y, Yamamoto Y, Fukunaga K. , et al. Comparative evaluation of 18F-FDG PET and 67Ga scintigraphy in patients with sarcoidosis. J Nucl Med 2006; 47 (10) 1571-1576
  • 78 Sobic-Saranovic D, Grozdic I, Videnovic-Ivanov J. , et al. The utility of 18F-FDG PET/CT for diagnosis and adjustment of therapy in patients with active chronic sarcoidosis. J Nucl Med 2012; 53 (10) 1543-1549
  • 79 Sohn M, Culver DA, Judson MA, Scott TF, Tavee J, Nozaki K. Spinal cord neurosarcoidosis. Am J Med Sci 2014; 347 (03) 195-198
  • 80 Flanagan EP. Autoimmune myelopathies. Handb Clin Neurol 2016; 133: 327-351
  • 81 Leavitt JA, Campbell RJ. Cost-effectiveness in the diagnosis of sarcoidosis: the conjunctival biopsy. Eye (Lond) 1998; 12 (Pt 6): 959-962
  • 82 Korkmaz Ekren P, Mogulkoc N, Toreyin ZN. , et al. Conjunctival biopsy as a first choice to confirm a diagnosis of sarcoidosis. Sarcoidosis Vasc Diffuse Lung Dis 2016; 33 (03) 196-200
  • 83 Pichler MR, Flanagan EP, Aksamit AJ, Leavitt JA, Salomão DR, Keegan BM. Conjunctival biopsy to diagnose neurosarcoidosis in patients with inflammatory nervous system disease of unknown etiology. Neurol Clin Pract 2015; 5 (03) 216-223
  • 84 Pettersen JA, Zochodne DW, Bell RB, Martin L, Hill MD. Refractory neurosarcoidosis responding to infliximab. Neurology 2002; 59 (10) 1660-1661
  • 85 O'Reilly MW, Sexton DJ, Dennedy MC. , et al. Radiological remission and recovery of thirst appreciation after infliximab therapy in adipsic diabetes insipidus secondary to neurosarcoidosis. QJM 2015; 108 (08) 657-659
  • 86 Gelfand JM, Bradshaw MJ, Stern BJ. , et al. Infliximab for the treatment of CNS sarcoidosis: a multi-institutional series. Neurology 2017; 89 (20) 2092-2100
  • 87 Rossman MD, Newman LS, Baughman RP. , et al. A double-blinded, randomized, placebo-controlled trial of infliximab in subjects with active pulmonary sarcoidosis. Sarcoidosis Vasc Diffuse Lung Dis 2006; 23 (03) 201-208
  • 88 Baughman RP, Drent M, Kavuru M. , et al; Sarcoidosis Investigators. Infliximab therapy in patients with chronic sarcoidosis and pulmonary involvement. Am J Respir Crit Care Med 2006; 174 (07) 795-802
  • 89 Bomprezzi R, Pati S, Chansakul C, Vollmer T. A case of neurosarcoidosis successfully treated with rituximab. Neurology 2010; 75 (06) 568-570
  • 90 Hamano H, Kawa S, Horiuchi A. , et al. High serum IgG4 concentrations in patients with sclerosing pancreatitis. N Engl J Med 2001; 344 (10) 732-738
  • 91 Stone JH. IgG4-related disease: nomenclature, clinical features, and treatment. Semin Diagn Pathol 2012; 29 (04) 177-190
  • 92 Carruthers MN, Khosroshahi A, Augustin T, Deshpande V, Stone JH. The diagnostic utility of serum IgG4 concentrations in IgG4-related disease. Ann Rheum Dis 2015; 74 (01) 14-18
  • 93 Carruthers R, Carruthers M, Della-Torre E. IgG4-related disease and other causes of inflammatory meningeal disease. Semin Neurol 2014; 34 (04) 395-404
  • 94 Deshpande V, Zen Y, Chan JK. , et al. Consensus statement on the pathology of IgG4-related disease. Mod Pathol 2012; 25 (09) 1181-1192
  • 95 Lindstrom KM, Cousar JB, Lopes MB. IgG4-related meningeal disease: clinico-pathological features and proposal for diagnostic criteria. Acta Neuropathol 2010; 120 (06) 765-776
  • 96 Carruthers MN, Topazian MD, Khosroshahi A. , et al. Rituximab for IgG4-related disease: a prospective, open-label trial. Ann Rheum Dis 2015; 74 (06) 1171-1177
  • 97 Miller JJ, Venna N, Siva A. Neuro-Behçet disease and autoinflammatory disorders. Semin Neurol 2014; 34 (04) 437-443
  • 98 Jubelt B, Mihai C, Li TM, Veerapaneni P. Rhombencephalitis / brainstem encephalitis. Curr Neurol Neurosci Rep 2011; 11 (06) 543-552
  • 99 Maldini C, Lavalley MP, Cheminant M, de Menthon M, Mahr A. Relationships of HLA-B51 or B5 genotype with Behcet's disease clinical characteristics: systematic review and meta-analyses of observational studies. Rheumatology (Oxford) 2012; 51 (05) 887-900
  • 100 International Team for the Revision of the International Criteria for Behçet's Disease (ITR-ICBD). The International Criteria for Behçet's Disease (ICBD): a collaborative study of 27 countries on the sensitivity and specificity of the new criteria. J Eur Acad Dermatol Venereol 2014; 28 (03) 338-347
  • 101 Kalra S, Silman A, Akman-Demir G. , et al. Diagnosis and management of Neuro-Behçet's disease: international consensus recommendations. J Neurol 2014; 261 (09) 1662-1676
  • 102 Moorthy RS, Inomata H, Rao NA. Vogt-Koyanagi-Harada syndrome. Surv Ophthalmol 1995; 39 (04) 265-292
  • 103 Lavezzo MM, Sakata VM, Morita C. , et al. Vogt-Koyanagi-Harada disease: review of a rare autoimmune disease targeting antigens of melanocytes. Orphanet J Rare Dis 2016; 11: 29
  • 104 Greco A, Fusconi M, Gallo A. , et al. Vogt-Koyanagi-Harada syndrome. Autoimmun Rev 2013; 12 (11) 1033-1038
  • 105 Levy-Clarke G, Jabs DA, Read RW, Rosenbaum JT, Vitale A, Van Gelder RN. Expert panel recommendations for the use of anti-tumor necrosis factor biologic agents in patients with ocular inflammatory disorders. Ophthalmology 2014; 121 (03) 785-96.e3
  • 106 Flores-Robles BJ, Blanco-Madrigal J, Sanabria-Sanchinel AA, Pascual DH, Demetrio-Pablo R, Blanco R. Anti-TNFα therapy and switching in severe uveitis related to Vogt-Koyanagi-Harada syndrome. Eur J Rheumatol 2017; 4 (03) 226-228
  • 107 Cuchacovich M, Solanes F, Díaz G. , et al. Comparison of the clinical efficacy of two different immunosuppressive regimens in patients with chronic Vogt-Koyanagi-Harada disease. Ocul Immunol Inflamm 2010; 18 (03) 200-207